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Development and Optimization of a Germination Assay and Long-Term Storage for Cannabis

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Development and Optimization of a Germination Assay and Long-Term Storage for Cannabis bioRxiv preprint doi: https://doi.org/10.1101/2020.03.19.999367; this version posted March 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. Development and optimization of a germination assay and long-term storage for Cannabis sativa pollen Daniel Gaudet1, Narendra Singh Yadav1, Aleksei Sorokin1, Andrii Bilichak1,2, Igor Kovalchuk1* 1 Department of Biological Sciences, University of Lethbridge, Lethbridge T1K 3M4, Alberta, Canada 2Current address: Morden Research and Development Center, Agriculture and Agri-Food Canada, Morden, MB, Canada * Corresponding author: [email protected] Abstract Pollen viability and storage is of great interest to cannabis breeders and researchers to maintain desirable germplasm for future use in breeding or for biotechnological and gene editing applications. Here, we report a simple and efficient cryopreservation method for long-term storage of Cannabis sativa pollen. Additionally, we have deciphered the bicellular nature of cannabis pollen using DAPI staining. We have also standardized a pollen germination assay to assess the viability of cannabis pollen, and found pollen collected from different principal growth stages exhibits different longevity. Finally, we developed a long-term storage method which includes pollen combination with baked whole wheat flower and desiccation under vacuum for cryopreservation. By using this method, we were able to maintain germination viability in liquid nitrogen after 4 months, suggesting potentially indefinite preservation of cannabis pollen. Keywords: Cannabis sativa, Pollen germination assay, Cryopreservation, Long-term storage, DAPI staining of germinated pollen, Vegetative nuclei, Sperm nuclei. bioRxiv preprint doi: https://doi.org/10.1101/2020.03.19.999367; this version posted March 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. Introduction Cannabis or hemp (Cannabis sativa L.) is an annual, primarily dioecious flowering plant. The center of origin is in Central Asia, and it has been bred for thousand of years for a variety of traits including fiber, oil, seed and drug use (Piluzza et al., 2013). Cannabis is a diploid plant (2n=20), males are defined by heterogametic chromosomes (XY) with homogametic (XX) conferring the female phenotype. Male plants produce flowers containing stamens producing pollen whereas female plants develop ovaries that produce seed following pollination. Female inflorescences are characterized by secretory hairs known as glandular trichomes which produce a resinous mix of cannabinoids and aromatic compounds that are valued for both medical therapeutics and recreational effects (Chandra and Lata, 2017). Pollen viability is of great interest to breeders and researchers alike. Breeding projects may wish to store pollen for extended periods of time, where high value genetic material may be stored for future use or for biotechnological and gene editing applications, which requires a quick and effective method of determining pollen viability (Zottini et al., 1997; Engelmann and Takagi, 2000; Choudhary et al., 2014). Fluorescent stains such as fluorescein diacetate (FDA) or fluorochromatic reaction test (FCR) have been previously reported for assessing pollen viability in cannabis (Zottini et al., 1997; Choudhary et al., 2014). Viability is not always correlated with germination, as pollen may retain the ability to metabolize, while losing it’s ability to germinate (Engelmann and Takagi, 2000). To better assess germination, we established a pollen germination assay (PGA) to estimate germination rates. We also adapted a DAPI stain to visualize pollen pre- and post-germination, and to establish whether Cannabis sativa was a bicellular or tricellular species, which to our knowledge has not been reported in the literature. Approximately 30% of angiosperms are known to be tricellular, with the male gametophyte sexually immature at the time bioRxiv preprint doi: https://doi.org/10.1101/2020.03.19.999367; this version posted March 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. of anthesis (Williams et al., 2014). We also used the PGA to test how storage and timing of pollen collection could influence germination rates. Pollen germination rates were assessed over a period when stored at 4◦C from males at different stages of floral development. Finally, we developed a simple procedure for the long-term storage of cannabis pollen using desiccation with baked whole wheat flower followed by cryopreservation which potentially maintain long-term viability of pollen for future use. Materials and Methods Plant material and growth conditions Cannabis sativa plants (strain name “Spice”, THC dominant) were grown under full spectrum 300- Watt LED grow lights (PrimeGarden) with 16 hrs light for vegetative growth and 12 hrs light for flowering at 22◦C. Pollen germination assay (PGA) Pollen germination media (PGM) The pollen germination assay was adapted from Schreiber & Dresselhau (2003) with some modification. The original protocol from Schreiber & Dresselhau (2003) employed 1% noble agar. In our study, we tested pollen germination media as liquid or combined with 1% agar. We found that liquid media resulted in better image acquisition and quantification of germination than solid media. During optimization of the Pollen Germination Assay (PGA), pollen concentrations of 0.1, 1 and 10 mg/mL were employed with the pollen diluted in PGM and incubated for 16 hr. A 2X PGM contained the following: 10% sucrose (BIOSHOP), 0.005% H3BO3 (Sigma), 10 mM CaCl2 (BIOSHOP), 0.05 mM KH2PO4 (Merk) and 6% PEG 4000 (Fluka). After bioRxiv preprint doi: https://doi.org/10.1101/2020.03.19.999367; this version posted March 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. ◦ components were added to distilled H2O, heated on a stir plate for 10 mins at 70 C then filter sterilized. A 1X working solution was prepared fresh each day by diluting in distilled H2O. Pollen collection and optimization of the PGA Pollen was obtained from flowering male Cannabis sativa plants using a vacuum manifold method (Johnson-Brousseau and McCormick, 2004). For the standardized PGA, 10 mg of cannabis pollen was combined with 1 mL of freshly prepared 1X PGM and diluted to 0.1 mg/mL. 200 µL was then pipetted into a 24-well tissue culture plate (Flat Bottom Cell+, Sarstedt) and sealed with parafilm. Plates were incubated in the dark at 22◦C for 16 hours and examined using an inverted light microscope (Zeiss Axio Observer Z1, Germany). Imaging and germination assessment Images were taken using phase contrast at 100x magnification. For each technical replicate, 8 images were taken to get an accurate representation of germination. Pollen germination percentages were calculated by dividing the number of germinating pollen grains by the total number of pollen grains. Germination percentages for each replicate represent the averages of the eight images. DAPI staining of cannabis pollen to decipher its bicellular or tricellular nature Collected pollen was stained with DAPI (4′,6-diamidino-2-phenylindole) and imaged using an inverted fluorescent microscope (Zeiss Axio Observer Z1). The DAPI staining protocol was adapted from Backues et al. (Backues et al., 2010). Germinated pollen was suspended in pollen isolation buffer (PIB) containing 100 mM NaPO4 (pH 7.5), 1 mM EDTA, 0.1% (v/v) Triton X-100 and 1 µg/ mL DAPI. A drop of solution was placed on a coverslip, incubated at room temperature for 5 minutes and viewed with the DAPI filter set. For DAPI staining of germinated pollen, pollen bioRxiv preprint doi: https://doi.org/10.1101/2020.03.19.999367; this version posted March 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. germination was performed as previously described, and staining was conducted with 1 µg/ mL DAPI after 16 hrs in PGM. Pollen collection from different development stages to assess the loss of pollen viability over time Pollen was collected from male Cannabis sativa plants at different stages of the flowering development. The four stages of flowering were chosen according to the BBCH (Biologische Bundesantalt, Bundessortenamt and Chemische) scale adapted for cannabis (Mishchenko et al., 2017) and are listed as follows with the BBCH notation in brackets: Early (62), Mid (64), Mid- Late (65) and Late (67). Early stage (62) flowering was characterized by green mostly (80%) unopened anthers. By Mid stage (64) approximately 40% of anthers were open while Mid-Late was characterized by 50% opened. By Late stage (68) flowering was over and many of the flowers had turned yellow and fallen. Following collection, an aliquot from each developmental stage was taken and used in the PGA for germination rate at time of collection (T0). The rest of the aliquots were stored in a 1.5 mL centrifuge tube at 4◦C in the dark. After one week an aliquot from the different developmental stages was used for a PGA (T1), again after 2 weeks (T2) and again after 3 weeks (T3). Cryopreservation of pollen Cannabis pollen submerged in Liquid Nitrogen (LN) without the use of any cryoprotectant or treatment will fail to germinate after the formation of ice crystals (Bajaj, 1987; Towill et al., 2000).
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